Proline oxidation fuels mitochondrial respiration during dark-induced leaf senescence in Arabidopsis thaliana.


Journal

Journal of experimental botany
ISSN: 1460-2431
Titre abrégé: J Exp Bot
Pays: England
ID NLM: 9882906

Informations de publication

Date de publication:
18 11 2019
Historique:
received: 09 04 2019
accepted: 18 07 2019
pubmed: 11 9 2019
medline: 11 8 2020
entrez: 11 9 2019
Statut: ppublish

Résumé

Leaf senescence is a form of developmentally programmed cell death that allows the remobilization of nutrients and cellular materials from leaves to sink tissues and organs. Among the catabolic reactions that occur upon senescence, little is known about the role of proline catabolism. In this study, the involvement in dark-induced senescence of proline dehydrogenases (ProDHs), which catalyse the first and rate-limiting step of proline oxidation in mitochondria, was investigated using prodh single- and double-mutants with the help of biochemical, proteomic, and metabolomic approaches. The presence of ProDH2 in mitochondria was confirmed by mass spectrometry and immunogold labelling in dark-induced leaves of Arabidopsis. The prodh1 prodh2 mutant exhibited enhanced levels of most tricarboxylic acid cycle intermediates and free amino acids, demonstrating a role of ProDH in mitochondrial metabolism. We also found evidence of the involvement and the importance of ProDH in respiration, with proline as an alternative substrate, and in remobilization of proline during senescence to generate glutamate and energy that can then be exported to sink tissues and organs.

Identifiants

pubmed: 31504781
pii: 5555536
doi: 10.1093/jxb/erz351
pmc: PMC6859731
doi:

Substances chimiques

Arabidopsis Proteins 0
Chlorophyll 1406-65-1
Proline 9DLQ4CIU6V

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6203-6214

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.

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Auteurs

Alban Launay (A)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Cécile Cabassa-Hourton (C)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Holger Eubel (H)

Institute of Plant Genetics, Plant Proteomics, Leibniz University Hannover, Hannover, Germany.

Régis Maldiney (R)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Anne Guivarc'h (A)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Emilie Crilat (E)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Séverine Planchais (S)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Jérôme Lacoste (J)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Marianne Bordenave-Jacquemin (M)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Gilles Clément (G)

Institut Jean-Pierre Bourgin, UMR 1318, INRA-AgroParisTech, Centre INRA Versailles, Versailles Cedex, France.

Luc Richard (L)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Pierre Carol (P)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Hans-Peter Braun (HP)

Institute of Plant Genetics, Plant Proteomics, Leibniz University Hannover, Hannover, Germany.

Sandrine Lebreton (S)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

Arnould Savouré (A)

Sorbonne Université, CNRS, IRD 242, INRA, PARIS 7, UPEC, Institut d'Ecologie et des Sciences de l'Environnement de Paris, iEES, Paris, France.

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Classifications MeSH